Causes of functional low vision in a Brazilian rehabilitation service

There is limited information on functional low vision (FLV) in Latin America, especially in individuals under 50 years of age. In the present study, we retrospectively evaluated the medical records of 1393 consecutive subjects seen at a Brazilian tertiary rehabilitation service, from February 2009 to June 2016. We collected sociodemographic, clinical data, and information on optical aids and spectacle prescription. Subjects were divided into three age groups: 0 to 14 years old (children), 15 to 49 years old (young adults), and 50 years or older (older adults). The main etiologies leading to FLV in children were cerebral visual impairment (27.9%), ocular toxoplasmosis (8.2%), and retinopathy of prematurity (7.8%). In young adults, retinitis pigmentosa (7.4%) and cone/rod dystrophy (6.5%) were the most frequent, while in older adults, age-related macular degeneration (25.3%) and diabetic retinopathy (18.0%) were the leading causes. Our results indicate that preventable diseases are important causes of FLV in children in the area, and proper prenatal care could reduce their burden. The increasing life expectancy in Latin America and the diabetes epidemic are likely to increase the demand for affordable, people-centered rehabilitation centers, and their integration into health services should be planned accordingly.


Scientific Reports
| (2022) 12:2807 | https://doi.org/10.1038/s41598-022-06798-0 www.nature.com/scientificreports/ area, since approximately 70% of the population use the public health service 8 , and our Rehabilitation Center is the only service in the region. In the present retrospective study, we describe the demographic profile, the causes of functional low vision and its frequencies, and the prescribed optical devices in a Brazilian rehabilitation service during its first 89 months of existence.

Methods
The study protocol adhered to the Declaration of Helsinki's tenets and was approved by the Ethics Committee in Human Research at Ribeirão Preto General Hospital (approval number 58577316. 8.0000.5440). In this retrospective study, data regarding scheduling and attendance from February 1st, 2009, through June 30th, 2016, were obtained from the hospital's electronic scheduling system and medical records. Subjects' demographics included age at the first appointment, sex, city of residence, and distance from the Rehabilitation Service. Medical history was obtained by the review of physical (n = 1382; 99.2%) and electronic medical charts (n = 11; 0.8%). Medical data obtained from physical or electronic medical records cannot be altered or deleted after medical care. All of the patients were assisted by either MMF or RA-F. All data of interest for this study was collected manually to an Excel sheet and then transferred to a software package 9 . The data included distance best-corrected visual acuity (BCVA), ophthalmological diagnosis of the better-seeing eye, anatomical site of the main diagnosis 10 , types of prescription (spectacles and optical devices), and its acquisition (out-of-pocket or donated by the institution). Optical devices were divided into magnifying loupes, telescopes, and spectacles with an addition equal to or greater than + 4.00 D and filtering lenses. For donated optical devices, the time elapsed from prescription to delivery was also analyzed. Inclusion criteria were subjects with distance BCVA < 6/18 to ≥ LP on the better-seeing eye due to untreatable causes (FLV) associated with a known etiology; and complete ophthalmological evaluation included VA, refractometry, slit-lamp examination, and fundoscopy. Children unable to inform VA were also included in the study. Children unable to inform VA, but with visual behavior compatible with low vision and any irreversible diagnosis were also included.
Exclusion criteria were subjects with incomplete or no ophthalmological evaluation, or when their BCVA was equal or better to 6/18, or no light perception in both eyes. Only one cause of FLV per subject was assigned (the primary diagnosis that led to FLV in the better-seeing eye). When there was a concomitant diagnosis of cerebral palsy and an ocular diagnosis that led to FLV (e.g., retinopathy of prematurity or optic nerve atrophy), the ocular diagnosis was chosen.
The subjects were divided into three age groups, according to Resnikoff et al. 11 0 to 14 years old (children), 15 to 49 years old (young adults), and subjects aged 50 years and older (older adults). Older adults were also subdivided into 50-59 years old, 60-69 years old, and 70 years or more. BCVA was measured using the Early Treatment Diabetic Retinopathy Study Chart (Lighthouse, Long Island, NY) and classified according to the International Statistical Classification of Diseases and Related Health Problems 10th Revision (ICD-10), World Health Organization 12 , as follows: moderate visual impairment (BCVA < 6/18 to 6/60); severe visual impairment (BCVA < 6/60 to 3/60); blindness (BCVA < 3/60 to 1/60); and blindness (BCVA < 1/60 to light perception). The anatomical site of the leading cause of functional low vision of the better seeing-eye was recorded for each included subject 10 . A category "retrobulbar" was created to accommodate central nervous system involvement cases, such as cerebral vision impairment, due to many etiologies, such as anoxia, malformations, and tumors.
Statistical analyses were performed using the statistical analysis system R: Core Team, Vienna, Austria 9 . Continuous variables were analyzed using the Mann-Whitney test. A p-value of less than 0.05 was considered to be statistically significant. Frequency tables were used for descriptive analysis.
Ethical approval. Due to the retrospective nature of this study, informed consent was not obtained from participants and legal guardians. The Ethics Committee in Human Research at Ribeirão Preto General Hospital approved the waiver for the consent (approval number 58577316.8.0000.5440).

Results
We identified scheduled appointments for 2168 subjects in our rehabilitation service during the study period. Among them, 252 (11.6%) did not attend the appointment, 442 were excluded due to BCVA equal or better to 6/18, 47 with no light perception in both eyes, and 34 were excluded due to incomplete ophthalmological evaluation, leaving 1393 subjects included for analysis ( Fig. 1).
Most of the included subjects were men (n = 727; 52.2%), and older adults corresponded to the most numerous group (n = 541; 38.8%), followed by children (n = 512; 36.7%; 236 of them younger than 5 years old). There was no sex predilection in all studied groups. Retina was the most frequent anatomical affected site (n = 655; 47.0%), followed by retrobulbar causes (n = 248; 17.8%), which included cerebral visual impairment as the main etiology (n = 143; 10.2% of the total) ( Table 1). Regarding the anatomical site of the main diagnosis, in subjects under 15 years of age (n = 512) most cases were identified as retrobulbar (n = 184; 35.9%), followed by retina (n = 154; 30.1%) and whole globe (n = 60; 11.7%). In the group 15-49 years (n = 340), retina was the most affected site (n = 154; 45.3%), followed by retrobulbar (n = 45; 13.2%) and optic nerve (n = 44; 12.9%). For the subjects with 50 years and more (n = 541), retina was also the most frequently affected site (n = 378; 69.9%), followed by the whole globe (n = 64; 11.8%) and the optic nerve (n = 37; 6.8%). Approximately one out of three examined subjects were from Ribeirão Preto (n = 424), and 62.4% (n = 869) were residents from cities within a range of 150 km from Ribeirão Preto. There were no differences in the distances from the city where they lived and the rehabilitation service between the subjects who attended and those who missed their first appointments (p = 0.09).

Discussion
In this study of a large series of 1393 subjects seen in a tertiary Brazilian rehabilitation service, we observed that most cases had diseases affecting the posterior segment (n = 768; 55.1%; retina and optic nerve combined, uveitis not included). Older adults received more optical devices prescription, while children received more spectacle prescriptions. The rate of optical device acquisition, either donated or purchased, was high in all groups, ranging from 73.4% in individuals aged 15-49 years old to 90.9% in older adults. Although the quality of life of the subjects included in the study was not assessed, our results suggest that young adults, subjects with moderate visual impairment, and subjects with cone/rod dystrophy and albinism benefited most from the rehabilitation center. Since the cost of the spectacles and optical devices can be a barrier for part of the population, especially in low-middle income countries like Brazil, identifying those who cannot afford the prescribed aid and providing affordable, low-cost spectacles and optical devices is paramount for proper rehabilitation.
Age-related macular degeneration, diabetic retinopathy, and glaucoma were the leading causes of FLV in individuals aged 50 years or older. This is in agreement with most Brazilian population-based studies [13][14][15][16] , although interestingly, diabetic retinopathy does not seem to be a major blinding condition in the Brazilian Amazon region 13 . Although diabetic retinopathy falls in second place as a cause of FLV in individuals aged 50 years or more, the disease is also present among the main causes in the 15-49 years group and was the leading cause of FLV in individuals 50-69 years old, reflecting an increased burden in economically-active individuals.
Retinopathy of prematurity, considered a leading cause of childhood blindness globally 17 and in Latin America 18 , was an important cause of FLV in children in the present study, but less frequent than CNS-associated disorders and ocular toxoplasmosis. Toxoplasmosis has a higher frequency and also a higher burden in Latin America than other regions of the world, and prophylactic measures related to water and food consumption and educational campaigns should target pregnant women in the region 19 . In other Brazilian studies, ocular toxoplasmosis and retinopathy of prematurity are also among the main diagnosis in children attending rehabilitation services 20,21 , whereas retinopathy of prematurity was the main diagnosis in a study conducted in children attending a Mexican low vision service 22 . This reinforces the need for actions to preventable diseases.
We found an extensive time between prescription and donation of optical devices (median: 10.8 months). It is important to emphasize that this waiting time occurred in the first years of the Rehabilitation Center's life, due to the difficulty in finding optical aid providers and combining the supply with the rules for releasing financial resources for this purpose by the public health system. This is a time-consuming process initially and needs to be continuously improved, so that the waiting time is as little as possible and patients can be effectively rehabilitated. We believe that the search for more suppliers and the reduction of bureaucracy for the use of public resources may substantially reduce this time interval. Table 3. Causes of functional low vision divided per age group (n = 1393). AMD Aged-Related Macular Disease, ROP Retinopathy of Prematurity, Cong Congenital. a Low vision with no defined etiology (6); acquired central nervous system infection (6); chronic uveitis associated with juvenile idiopathic arthritis (1). b Low vision with no defined etiology (12); nystagmus (8) ocular malformation (8); central nervous system infection (7); central nervous system stroke (5); cerebellar ataxia (5); traumatic brain injury (4); amblyopia due to high ametropia (2); acquired choroidopathy (3); ocular trauma (3), cerebral palsy (2); ocular tumor (1); sympathetic ophthalmia (1). c Low vision with no defined etiology (9); central nervous system stroke (7); ocular trauma (4); uveitis with no defined etiology (2); traumatic brain injury (2); amblyopia due to high ametropia (1); ischemic ocular syndrome (1); congenital infection (1); ocular malformation (1).   www.nature.com/scientificreports/ Strengths of our study include the substantial number of enrolled subjects, the inclusion of all age groups, information on different VA categories, and also prescribed/donated spectacle correction and optical devices. Limitations of the work reflect its retrospective nature, including the inability to assess refractive error data and some ocular findings, for example disc pallor in children. Also, we were unable to assess the adherence to the use of donated spectacles and optical devices, and whether the subjects use any electronic devices, such as cell phone cameras as a magnifying glass and mobile apps for low vision 23 . This study was conducted at a tertiary referral public hospital clinic, and the exact causes of functional low vision and their importance in the sample may not reflect the reality in the region, since there are many barriers in access to public health care and part of the population uses the private health system 8 . Future studies including longitudinal component and multidisciplinary approach in rehabilitation centers to provide holistic healthcare to people with visual impairment are needed.
Our results indicate that preventable diseases are important causes of functional low vision in children in the area, and proper prenatal care and educational campaigns could reduce their burden. The increasing life expectancy in Brazil and most Latin American countries 24 and the diabetes epidemic 25 are likely to increase the demand for affordable, people-centered rehabilitation centers, and their integration into health services should be planned accordingly.